Three rare diseases in one Sib pair: RAI1, PCK1, GRIN2B mutations associated with Smith-Magenis Syndrome, cytosolic PEPCK deficiency and NMDA receptor glutamate insensitivity

Molecular Genetics and Metabolism

Volumn 113, Issue 3, 2014, Pages 161-170

  Adams, David R ^a,b   Yuan, Hongjie ^c   Holyoak, Todd ^d   Arajs, Katrina H ^d   Hakimi, Parvin ^f,g   Markello, Thomas C ^a   Wolfe, Lynne A ^a   Vilboux, Thierry ^b   Burton, Barbara K ^e,l   Fajardo, Karin Fuentes ^a   Grahame, George ^h   Holloman, Conisha ⁱ   Sincan, Murat ^a   Smith, Ann C M ^a   Wells, Gordon A ^j,k   Huang, Yan ^a   Vega, Hugo ^a   Snyder, James P ^j   Golas, Gretchen A ^a   Tifft, Cynthia J ^a   Boerkoel, Cornelius F ^a   Hanson, Richard W ^f   Traynelis, Stephen F ^c   Kerr, Douglas S ^f,g,h   Gahl, William A ^a,b   more..

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WATERLOO   (Canada)

^e NORTHWESTERN UNIVERSITY   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

^g CASE WESTERN RESERVE UNIVERSITY   (United States)

^h CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^j UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^k EMORY UNIVERSITY   (United States)

^l STELLENBOSCH UNIVERSITY   (South Africa)

more..

Author keywords

Developmental delay; Dysmorphism; Hypoglycemia; Lactic acidemia; Multiple genetic disorders; Protein structure function

Indexed keywords

DNA; FRUCTOSE BISPHOSPHATASE; GLUCOSE; GLUCOSE 1 PHOSPHATE; GLUCOSE 6 PHOSPHATASE; GLUTAMIC ACID; GROWTH HORMONE; HYDROCORTISONE; INSULIN; LACTIC ACID; MILK PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PHOSPHORYLASE; PHOSPHORYLASE KINASE; PYRUVATE CARBOXYLASE; PYRUVATE DEHYDROGENASE; SOYBEAN PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; PCK1 PROTEIN, HUMAN; PCK2 PROTEIN, HUMAN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); RAI1 PROTEIN, HUMAN; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR;

ALLERGY; ARTICLE; ASHKENAZI JEW; BIRTH WEIGHT; BODY HEIGHT; BODY MASS; BRACHYCEPHALY; BRACHYDACTYLY; CASE REPORT; CLINODACTYLY; COARSE FACE; CONGENITAL DISORDER; CYTOSOLIC PEPCK DEFICIENCY; DEVELOPMENTAL DISORDER; ELECTROMYOGRAM; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ESOPHAGITIS; EXOME; FASTING HYPOGLYCEMIA; FATIGUE; FATTY ACID OXIDATION; FEVER; FLATFOOT; GASTROESOPHAGEAL REFLUX; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLYCOGEN ANALYSIS; GLYCOGEN STORAGE DISEASE; GROWTH HORMONE BLOOD LEVEL; HAND MOVEMENT; HEAD CIRCUMFERENCE; HISTOPATHOLOGY; HUMAN; HYDROCORTISONE BLOOD LEVEL; HYPOGLYCEMIA; HYPOTELORISM; INSULIN BLOOD LEVEL; INTELLECTUAL IMPAIRMENT; KETONURIA; LACTIC ACIDEMIA; LACTIC ACIDOSIS; LETHARGY; LIVER BIOPSY; LIVER FIBROSIS; MEDICAL HISTORY; MOTOR DEVELOPMENT; MUSCLE BIOPSY; MUSCLE HYPOTONIA; MUSCLE TONE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUTAMATE INSENSITIVITY; NEUROPATHY; NEUROPSYCHIATRY; NEWBORN PERIOD; NONSENSE MUTATION; OBESITY; PREMATURE LABOR; SIBLING; SLEEP DISORDER; SMITH MAGENIS SYNDROME; STEATOSIS; STEREOTYPY; STRIA; TRANSIENT UNEXPLAINED NEUROPATHY; UNSTEADY GAIT; URINE LEVEL; AMINO ACID SEQUENCE; CHILD; DEFICIENCY; FEMALE; GENETIC ASSOCIATION; GENETICS; HEK293 CELL LINE; MISSENSE MUTATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; SMITH-MAGENIS SYNDROME;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; DNA MUTATIONAL ANALYSIS; FEMALE; GENETIC ASSOCIATION STUDIES; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, N-METHYL-D-ASPARTATE; SMITH-MAGENIS SYNDROME; TRANSCRIPTION FACTORS;

EID: 84914159262     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2014.04.001     Document Type: Article

References (52)

1. Guy E.L., Peckham D.G., Brownlee K.G., Conway S.P., Lee T.W. Cystic fibrosis co-existing with trisomy 21. J. Cyst. Fibros. 2010, 9:330-331.
2. Marin S., Casano-Sancho P., Villarreal-Pena N., Sebastiani G., Pinillos S., Perez-Duenas B., Hwa V., Rosenfeld R.G., Ibanez L. Triple A syndrome in a patient with genetic growth hormone insensitivity: phenotypic effects of two genetic disorders. Horm. Res. Paediatr. 2012, 77:63-68.
3. Gahl W.A., Boerkoel C.F., Boehm M. The NIH Undiagnosed Diseases Program: bonding scientists and clinicians. Dis. Model. Mech. 2012, 5:3-5.
4. Gahl W.A., Markello T.C., Toro C., Fajardo K.F., Sincan M., Gill F., Carlson-Donohoe H., Gropman A., Pierson T.M., Golas G., Wolfe L., Groden C., Godfrey R., Nehrebecky M., Wahl C., Landis D.M., Yang S., Madeo A., Mullikin J.C., Boerkoel C.F., Tifft C.J., Adams D. The National Institutes of Health Undiagnosed Diseases Program: insights into rare diseases. Genet. Med. 2012, 14:51-59.
5. Gahl W.A., Tifft C.J. The NIH Undiagnosed Diseases Program: lessons learned. JAMA 2011, 305:1904-1905.
6. Carr I.M., Markham S.A., Pena S.D. Estimating the degree of identity by descent in consanguineous couples. Hum. Mutat. 2011, 32:1350-1358.
7. Markello T.C., Han T., Carlson-Donohoe H., Ahaghotu C., Harper U., Jones M., Chandrasekharappa S., Anikster Y., Adams D.R., NISC Comparative Sequencing Program, Gahl W.A., Boerkoel C.F. Recombination mapping using Boolean logic and high-density SNP genotyping for exome sequence filtering. Mol. Genet. Metab. 2012, 105:382-389.
8. Adams D.R., Sincan M., Fuentes Fajardo K., Mullikin J.C., Pierson T.M., Toro C., Boerkoel C.F., Tifft C.J., Gahl W.A., Markello T.C. Analysis of DNA sequence variants detected by high-throughput sequencing. Hum. Mutat. 2012, 33:599-608.
9. Teer J.K., Bonnycastle L.L., Chines P.S., Hansen N.F., Aoyama N., Swift A.J., Abaan H.O., Albert T.J., NISC Comparative Sequencing Program, Margulies E.H., Green E.D., Collins F.S., Mullikin J.C., Biesecker L.G. Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Res. 2010, 20:1420-1431.
10. Livak K. Comparative Ct Method 1997, Applied Biosystems, Inc., Grand Island, NY.
11. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
12. Low C.M., Zheng F., Lyuboslavsky P., Traynelis S.F. Molecular determinants of coordinated proton and zinc inhibition of N-methyl-d-aspartate NR1/NR2A receptors. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11062-11067.
13. Hedegaard M., Hansen K.B., Andersen K.T., Brauner-Osborne H., Traynelis S.F. Molecular pharmacology of human NMDA receptors. Neurochem. Int. 2012, 61:601-609.
14. Traynelis S.F., Burgess M.F., Zheng F., Lyuboslavsky P., Powers J.L. Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J. Neurosci. 1998, 18:6163-6175.
15. Burger P.B., Yuan H., Karakas E., Geballe M., Furukawa H., Liotta D.C., Snyder J.P., Traynelis S.F. Mapping the binding of GluN2B-selective N-methyl-d-aspartate receptor negative allosteric modulators. Mol. Pharmacol. 2012, 82:344-359.
16. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R.D., Kale L., Schulten K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26:1781-1802.
17. Atkin B.M., Utter M.F., Weinberg M.B. Pyruvate carboxylase and phosphoenolpyruvate carboxykinase activity in leukocytes and fibroblasts from a patient with pyruvate carboxylase deficiency. Pediatr. Res. 1979, 13:38-43.
18. Kerr D.S., Ho L., Berlin C.M., Lanoue K.F., Towfighi J., Hoppel C.L., Lusk M.M., Gondek C.M., Patel M.S. Systemic deficiency of the first component of the pyruvate dehydrogenase complex. Pediatr. Res. 1987, 22:312-318.
19. Hakimi P., Yang J., Casadesus G., Massillon D., Tolentino-Silva F., Nye C.K., Cabrera M.E., Hagen D.R., Utter C.B., Baghdy Y., Johnson D.H., Wilson D.L., Kirwan J.P., Kalhan S.C., Hanson R.W. Overexpression of the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) in skeletal muscle repatterns energy metabolism in the mouse. J. Biol. Chem. 2007, 282:32844-32855.
20. Johnson T.A., Holyoak T. The Omega-loop lid domain of phosphoenolpyruvate carboxykinase is essential for catalytic function. Biochemistry 2012, 51:9547-9559.
21. Johnson T.A., Holyoak T. Increasing the conformational entropy of the Omega-loop lid domain in phosphoenolpyruvate carboxykinase impairs catalysis and decreases catalytic fidelity. Biochemistry 2010, 49:5176-5187.
22. Bailey S. The Ccp4 suite - programs for protein crystallography. Acta Crystallogr. 1994, D50:760-763.
23. Sullivan S.M., Holyoak T. Enzymes with lid-gated active sites must operate by an induced fit mechanism instead of conformational selection. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13829-13834.
24. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30:1022-1025.
25. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. 2004, D60:2126-2132.
26. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:12-21.
27. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., Richardson D.C. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
28. Vilboux T., Ciccone C., Blancato J.K., Cox G.F., Deshpande C., Introne W.J., Gahl W.A., Smith A.C., Huizing M. Molecular analysis of the Retinoic Acid Induced 1 gene (RAI1) in patients with suspected Smith-Magenis syndrome without the 17p11.2 deletion. PLoS One 2011, 6:e22861.
29. Hanson R.W. Thematic minireview series: a perspective on the biology of phosphoenolpyruvate carboxykinase 55years after its discovery. J. Biol. Chem. 2009, 284:27021-27023.
30. Vidnes J., Sovik O. Gluconeogenesis in infancy and childhood. III. Deficiency of the extramitochondrial form of hepatic phosphoenolpyruvate carboxykinase in a case of persistent neonatal hypoglycaemia. Acta Paediatr. Scand. 1976, 65:307-312.
31. Furukawa H., Singh S.K., Mancusso R., Gouaux E. Subunit arrangement and function in NMDA receptors. Nature 2005, 438:185-192.
32. Vance K.M., Simorowski N., Traynelis S.F., Furukawa H. Ligand-specific deactivation time course of GluN1/GluN2D NMDA receptors. Nat. Commun. 2011, 2:294.
33. Tarabeux J., Kebir O., Gauthier J., Hamdan F.F., Xiong L., Piton A., Spiegelman D., Henrion É., Millet B., S2D Team, Fathalli F., Joober R., Rapoport J.L., DeLisi L.E., Fombonne E., Mottron L., Forget-Dubois N., Boivin M., Michaud J.L., Drapeau P., Lafreniere R.G., Rouleau G.A., Krebs M.O. Rare mutations in N-methyl-d-aspartate glutamate receptors in autism spectrum disorders and schizophrenia. Transl. Psychiatry 2011, 1:e55.
34. de Ligt J., Willemsen M.H., van Bon B.W., Kleefstra T., Yntema H.G., Kroes T., Vulto-van Silfhout A.T., Koolen D.A., de Vries P., Gilissen C., del Rosario M., Hoischen A., Scheffer H., de Vries B.B., Brunner H.G., Veltman J.A., Vissers L.E. Diagnostic exome sequencing in persons with severe intellectual disability. N. Engl. J. Med. 2012, 367:1921-1929.
35. Endele S., Rosenberger G., Geider K., Popp B., Tamer C., Stefanova I., Milh M., Kortum F., Fritsch A., Pientka F.K., Hellenbroich Y., Kalscheuer V.M., Kohlhase J., Moog U., Rappold G., Rauch A., Ropers H.H., von Spiczak S., Tonnies H., Villeneuve N., Villard L., Zabel B., Zenker M., Laube B., Reis A., Wieczorek D., Van Maldergem L., Kutsche K. Mutations in GRIN2A and GRIN2B encoding regulatory subunits of NMDA receptors cause variable neurodevelopmental phenotypes. Nat. Genet. 2010, 42:1021-1026.
36. Epi K.C., P.Epilepsy Phenome/Genome, Allen A.S., Berkovic S.F., Cossette P., Delanty N., Dlugos D., Eichler E.E., Epstein M.P., Glauser T., Goldstein D.B., Han Y., Heinzen E.L., Hitomi Y., Howell K.B., Johnson M.R., Kuzniecky R., Lowenstein D.H., Lu Y.F., Madou M.R., Marson A.G., Mefford H.C., Esmaeeli Nieh S., O'Brien T.J., Ottman R., Petrovski S., Poduri A., Ruzzo E.K., Scheffer I.E., Sherr E.H., Yuskaitis C.J., Abou-Khalil B., Alldredge B.K., Bautista J.F., Berkovic S.F., Boro A., Cascino G.D., Consalvo D., Crumrine P., Devinsky O., Dlugos D., Epstein M.P., Fiol M., Fountain N.B., French J., Friedman D., Geller E.B., Glauser T., Glynn S., Haut S.R., Hayward J., Helmers S.L., Joshi S., Kanner A., Kirsch H.E., Knowlton R.C., Kossoff E.H., Kuperman R., Kuzniecky R., Lowenstein D.H., McGuire S.M., Motika P.V., Novotny E.J., Ottman R., Paolicchi J.M., Parent J.M., Park K., Poduri A., Scheffer I.E., Shellhaas R.A., Sherr E.H., Shih J.J., Singh R., Sirven J., Smith M.C., Sullivan J., Lin Thio L., Venkat A., Vining E.P., Von Allmen G.K., Weisenberg J.L., Widdess-Walsh P., Winawer M.R. De novo mutations in epileptic encephalopathies. Nature 2013, 501:217-221.
37. Freunscht I., Popp B., Blank R., Endele S., Moog U., Petri H., Prott E.C., Reis A., Rubo J., Zabel B., Zenker M., Hebebrand J., Wieczorek D. Behavioral phenotype in five individuals with de novo mutations within the GRIN2B gene. Behav. Brain Funct. 2013, 9:20.
38. Kenny E.M., Cormican P., Furlong S., Heron E., Kenny G., Fahey C., Kelleher E., Ennis S., Tropea D., Anney R., Corvin A.P., Donohoe G., Gallagher L., Gill M., Morris D.W. Excess of rare novel loss-of-function variants in synaptic genes in schizophrenia and autism spectrum disorders. Mol. Psychiatry 15 October 2013.
39. Lemke J.R., Hendrickx R., Geider K., Laube B., Schwake M., Harvey R.J., James V.M., Pepler A., Steiner I., Hortnagel K., Neidhardt J., Ruf S., Wolff M., Bartholdi D., Caraballo R., Platzer K., Suls A., De Jonghe P., Biskup S., Weckhuysen S. GRIN2B mutations in west syndrome and intellectual disability with focal epilepsy. Ann. Neurol. 2014, 75:147-154.
40. Myers R.A., Casals F., Gauthier J., Hamdan F.F., Keebler J., Boyko A.R., Bustamante C.D., Piton A.M., Spiegelman D., Henrion E., Zilversmit M., Hussin J., Quinlan J., Yang Y., Lafreniere R.G., Griffing A.R., Stone E.A., Rouleau G.A., Awadalla P. A population genetic approach to mapping neurological disorder genes using deep resequencing. PLoS Genet. 2011, 7:e1001318.
41. O'Roak B.J., Vives L., Girirajan S., Karakoc E., Krumm N., Coe B.P., Levy R., Ko A., Lee C., Smith J.D., Turner E.H., Stanaway I.B., Vernot B., Malig M., Baker C., Reilly B., Akey J.M., Borenstein E., Rieder M.J., Nickerson D.A., Bernier R., Shendure J., Eichler E.E. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 2012, 485:246-250.
42. Talkowski M.E., Rosenfeld J.A., Blumenthal I., Pillalamarri V., Chiang C., Heilbut A., Ernst C., Hanscom C., Rossin E., Lindgren A.M., Pereira S., Ruderfer D., Kirby A., Ripke S., Harris D.J., Lee J.H., Ha K., Kim H.G., Solomon B.D., Gropman A.L., Lucente D., Sims K., Ohsumi T.K., Borowsky M.L., Loranger S., Quade B., Lage K., Miles J., Wu B.L., Shen Y., Neale B., Shaffer L.G., Daly M.J., Morton C.C., Gusella J.F. Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell 2012, 149:525-537.
43. Constantine-Paton M. Effects of NMDA receptor antagonists on the developing brain. Psychopharmacol. Bull. 1994, 30:561-565.
44. Feldmeyer D., Cull-Candy S. Functional consequences of changes in NMDA receptor subunit expression during development. J. Neurocytol. 1996, 25:857-867.
45. Kutsuwada T., Sakimura K., Manabe T., Takayama C., Katakura N., Kushiya E., Natsume R., Watanabe M., Inoue Y., Yagi T., Aizawa S., Arakawa M., Takahashi T., Nakamura Y., Mori H., Mishina M. Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice. Neuron 1996, 16:333-344.
46. Loftis J.M., Janowsky A. The N-methyl-d-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol. Ther. 2003, 97:55-85.
47. Ozawa S., Kamiya H., Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 1998, 54:581-618.
48. Vallano M.L. Developmental aspects of NMDA receptor function. Crit. Rev. Neurobiol. 1998, 12:177-204.
49. Williams K., Russell S.L., Shen Y.M., Molinoff P.B. Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 1993, 10:267-278.
50. Yang J., Kalhan S.C., Hanson R.W. What is the metabolic role of phosphoenolpyruvate carboxykinase?. J. Biol. Chem. 2009, 284:27025-27029.
51. Steinberg M.H., Sebastiani P. Genetic modifiers of sickle cell disease. Am. J. Hematol. 2012, 87:795-803.
52. Sobolevsky A.I., Rosconi M.P., Gouaux E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 2009, 462:745-756.